Natural Selection

First published Sat Jun 7, 2008

Darwin's theory of evolution by natural selection provided the
first, and only, causal-mechanistic account of the existence of
adaptations in nature. As such, it provided the first, and only,
scientific alternative to the “argument from design”.
That alone would account for its philosophical significance. But the
theory also raises other philosophical questions not encountered in
the study of the theories of physics. Unfortunately the concept of
natural selection is intimately intertwined with the other basic
concepts of evolutionary theory—such as the concepts of fitness
and adaptation—that are themselves philosophically
controversial. Fortunately we can make considerable headway in getting
clear on natural selection without solving all of those outstanding
problems.

The theory of evolution by natural selection forms a central part of
modern evolutionary theory. There is some controversy among
biologists as to just how important natural selection is compared to
other processes producing evolutionary change, but there is no
controversy over the proposition that natural selection is
important. Some good might come of the efforts to produce a
general selection theory that would include the natural selection that
occurs as a part of the evolutionary process as a special case (e.g.
Hull 2001), but here the focus will be solely on the evolutionary
process.

Biology starts when reproduction begins. Stars may be said to
evolve, but they do not reproduce and so biological theory does not
apply to them. Biological evolution requires reproducing entities
that form lineages. It is these lineages that evolve. Thus
it is only within such lineages that we will properly apply the term
natural selection. A kindergarten class may certainly select
among different colored candies, but since those candies are not part
of self-reproducing lineages, we should not confuse this selection
process with natural selection.

Natural selection is a causal process. Distinguishing it from other
processes in evolution is one of major conceptual and empirical
problems of evolutionary biology. The bare bones of Darwin's
theory of evolution by natural selection are elegantly
simple. Typically (but not necessarily) there is
variation among organisms within a reproducing
population. Oftentimes (but not always) this variation is (to some
degree) heritable. When this variation is
causally connected to differential ability to survive and
reproduce, differential reproduction will
probably ensue. This last claim is one way of stating the
Principle of Natural Selection (from here on PNS). The PNS goes beyond
the causally neutral statement that is sometimes listed as the third
of what are often called “Darwin's Three
Conditions”, viz., different variants sometimes reproduce at
different rates. That statement leaves open the question of whether or
not the variation in question is causally responsible for the
differential reproduction. It leaves open the question of whether a
qualitatively similar outcome would result from repeated iterations of
this set-up. It leaves open the question of whether this process is
natural selection or drift (see below). It—the causally neutral
statement—does not suffice to state Darwin's
causal theory. Darwin clearly recognized this (see, for
example 1871) as did Lewontin (1978); although many contemporary
commentators fail to see this.

Why is it that some variants leave more offspring than others?
In those cases we label natural selection, it is because those variants
are better adapted, or are fitter than their
competitors. Thus we can define natural selection as
follows: Natural selection is differential reproduction due to
differential fitness (or differential adaptedness) within a
common selective environment (see next section). This definition
makes the concept of natural selection dependent on that of fitness,
which is unfortunate since many philosophers find the concept of
fitness deeply mysterious (see e.g., Ariew and Lewontin
2004). But like it or not, that is the way the theory is
structured. And, fortunately, we can make considerable headway in
understanding natural selection without solving all of the
philosophical problems surrounding the concept of fitness.

As a causal theory natural selection locates the causally relevant
differences that lead to differential reproduction. These differences
are differences in organisms' fitness to their environment. Or,
more fully, they are differences in various organismic capacities to
survive and reproduce in their environment. When these differences in
capacities are heritable, then evolution will (usually) ensue. This
sort of case must be carefully distinguished from cases where the
causes of differential reproduction are not located in the organisms,
but rather in their different environments. Let us make this
distinction more concrete. Imagine two genotypes of an annual plant
that grows in dense patches. Sunlight is at a premium and taller
plants shade shorter plants thus garnering more energy for growth and
reproduction. One genotype, G1, grows more quickly at
germination than the other, G2. Thus G1s
are initially taller than G2s and this difference
persists throughout the growing season due to G1s
increased energy stores. The consequence of this is that
G1s produce more flowers, more pollen and more seeds
than G2s. This is natural selection at work.

In contrast, imagine two genotypes of the same species,
G3 and G4 that do not differ in germination date,
growth rate, resource allocation between growth and reproduction or any
other factor relevant to reproduction when grown in a common
environment. Now imagine that seeds of these two genotypes are
distributed randomly across a patchwork of two quite different soil
types, call them E1 and E2. E1 and E2 are identical except that
E1 contains high levels of lead whereas E2 does not. Lead
dramatically and equally reduces growth and reproduction in both
G3 and G4. Finally imagine that this random
distribution process results in a correlation between genotype and
environment—i.e., G3s are disproportionately
found in E1. In consequence of all of this, G4s
produce more flowers, more pollen and more seeds than
G3s. But natural selection is
not occurring here. (Indeed this is a type of
drift, see below.)

In both cases differential reproduction occurs, and in both cases I
have already sketched causal explanations of this. In neither
case is differential reproduction mysterious (although chance does play
a role in the second explanation, but not the first). But only
the first case could result in adaptive
evolution. (See Brandon 1990, chapter 2 for fuller
discussion.) Biologists have long recognized the importance
of the difference discussed above, thus the importance of so-called
“common garden” experiments in experimental evolutionary
genetics. (In common garden experiments, the environments in
which different genotypes are placed are controlled as far as
possible. Furthermore, when environmental control is imperfect,
statistical techniques, in particular the analysis of variances and
covariances, are employed to separate out the effects of genotype vs.
environment.)

Clearly the two cases sketched above are highly simplified, and it
might be objected that nature is unlikely to contain many examples that
either model exactly applies to. This objection has both
epistemological and ontological sides. The epistemological side
of the objection has, I think, been met. First, the statistical
techniques mentioned in the last paragraph mitigate the force of
it. Even in messy cases biologists are fairly successful in
separating out environmental causes from genetic, or organismic, causes
of differential reproduction. (It should at least be mentioned
here that this sort of analysis also often yields genotype by
environment interactions, G × E. This occurs when, in
contrast to case 2, the relative performance of different genotypes
differs in different environments. Although common in nature, and
very important, we can ignore that here.) Second, the
experimental techniques and conceptual resources developed by
Antonovics et al. (1988), Brandon (1990) and Brandon and Antonovics
(1996) allow for precise measurements of environmental heterogeneity in
real life populations.

Ontologically the objection is this: when measured precisely
enough each organism lives in a unique environment. Thus if
natural selection requires multiple organisms competing in a common
selective environment, then it never really occurs. That,
if true, would be a serious objection to the picture of natural
selection I am presenting here. But I think we have very good
reason to believe it is not true. Unfortunately, here I can
present only the briefest sketch of it. What natural selection
explanations require is consistent ordinal relations in fitness of the
competing types—they do not require precise agreement of absolute
fitnesses of the competing types. Lots of empirical studies of
natural selection in the wild have shown consistent ordinal fitness
relations (see Endler 1986). Furthermore, the fact of adaptive
evolution, the consistent and persistent increase of one type over
others in evolutionary history, requires these consistent ordinal
relations, or what I have termed “common selective
neighborhoods”. Thus I think the ontological objection has
been met as well.

The short answer to this question is
“Yes”. I have already offered arguments in favor of
that answer. However the longer more complete answer is
“No, no, but yes”. I will explain.

There are two reasonable arguments that suggest a negative answer to
our question. I will review them both. In the beginning of
this essay I stated that considerable progress could be made in
articulating a clear and adequate conception of natural selection
without solving all of the philosophical problems associated with the
notion of fitness. However, in this section I will have to make
certain assumptions about fitness in order to address the issues to be
raised. The assumptions are quite plausible, but not
defensible in a short essay of this sort.

One negative answer is based on a radical rethinking of the problem
nature presents to evolving entities. Mainstream evolutionary
biology measures fitness in terms of reproductive success.
(Exactly how it defines fitness will not be addressed
here.) Survival is important exactly insofar as it contributes to
reproduction. Evolutionary success is reproductive success.
But suppose we turn the relation between reproduction and survival on
its head and think of reproduction as important only insofar as it
contributes to lineage survival. The fundamental evolutionary
problem is persistence, and reproduction is but one means of achieving
that (Bouchard 2004). Compare two lineages, one composed of
short-lived organisms that reproduce every year, the other composed of
organisms that live for 1,000+ years, but reproduce only rarely.
At the end of a thousand year period the first may have gone extinct,
while the second persists in virtue of simply surviving without
reproduction. Isn't this radical view just as defensible as
the more mainstream view? If so, then differential persistence
would count as natural selection, and differential reproduction would
not be necessary for natural selection to occur.

Interesting as this view is, I reject it because, with Dawkins
(1982), I believe that reproduction, in particular going through a
single cell bottle neck from whence the developmental process is
started anew, is necessary for the evolutionary process of
adaptation. Only by restarting the developmental process each
generation can fundamental alterations of that process be
achieved. Consider a grove of aspens that grows vertically
(in what we intuitively think of as trees) and horizontally by
underground runners that produce more “trees”. The
phenotype of the whole grove can change through time—growing
vigorously here, not growing there. But consider a genetic
mutation that would fundamentally alter Aspen phenotype. It may
occur in a multicellular runner. If so, it will be incorporated
in the resultant cell lineage. But that cell lineage will be one
of many in the next “tree” produced, since the next tree
grows not from a single cell, but from a multi-cell runner. Thus
the resultant “tree” will be a chimera, and not
fundamentally different from the others in the grove. In
contrast, were the runners single-celled at any cross-section, then a
somatic mutation would be incorporated in the whole of the downstream
“tree”. This, according to Harper (1977) and Dawkins
(1982), would count as reproduction, not growth, because this could
fundamentally rearrange Aspen development. (But that is not the
way Aspens grow.) Accordingly, the evolution of complex
adaptations, fundamental rearrangements of development, requires
differential reproduction.

A second reason to answer our question in the negative comes from a
(quite appropriate) focus on the ecological process of selection.
For practical reasons, many studies of natural selection in the wild
focus on only a small part of the life cycle. For instance, in
the most famous such study H. B. D. Kettlewell (1955, 1956) marked
different morphs of the peppered moth, Biston betularia,
released them (into polluted woods in one treatment, non-polluted woods
in another) and then recaptured them three days later. The
difference in the proportion of dark to light forms in the recaptured
vs. the released groups was taken to measure natural selection in
action. As Rudge (1999) points out, Kettlewell had preformed
numerous auxiliary studies to justify this inference, but for present
concerns what is crucial is that Kettlewell looked at only a small
portion of the entire life cycle, and in particular a portion that did
not involve reproduction. It is beyond the scope of this essay to
critically examine Kettlewell's actual work, but let us use it as
a basis to construct two hypothetical examples.

The first example mirrors the situation with which Kettlewell was
actually dealing. Let us suppose that there are two genetically
distinct morphs in a population of moths, call them Light and
Dark. In survivorship through the larval stage both forms are
identical. They are also identical in fertility and
fecundity. They differ only in survivorship during the adult
stage prior to mating. This difference is due to a difference in
their conspicuousness to birds as they rest on the trunks of
trees. On dark trees the Darks are less conspicuous than Lights,
and vice versa on light trees. In a polluted wood, most of the
tree trunks are dark. A biologist marks equal numbers of Darks
and Lights, releases them into the polluted woods and recaptures them
three days later. She recaptures twice as many Darks as
Lights. Based on her knowledge of when pollution was introduced
into the woods, the frequency of the two morphs in woods that have not
been polluted, the underlying genetics of the two morphs, and her
observed selection differential between them, she builds a population
genetic model of the situation that predicts a relative frequency of
the two morphs for the present. That prediction fits the observed
frequencies. She concludes that her mark-release-recapture
experiment has captured natural selection in action. I, and
the vast majority of evolutionary biologists, would agree with this
conclusion.

In contrast, imagine a second example. It is just like the
first except that in the larval stage the Lights out survive the Darks
by a two to one margin. This difference in survival in the larval
stage exactly counterbalances the difference in survival in the adult
stage, leading to no difference in reproductive
success between the two morphs. Were this going on we
couldn't explain the match between frequencies observed in
different woods and the selective processes occurring in the adult
stage. But that is not crucial to our question. The
question for us is: Are the two processes observed in the
mark-release-recapture studies in our hypothetical cases both examples
of natural selection?

If you think, as has been suggested, that natural selection requires
differential reproduction, then you must say that the second example is
not one of natural selection. But one might object to this
conclusion as follows. The ecological process of birds
preying on moths based on their relative conspicuousness is exactly the
same in the two examples. That ecological process was identified
as natural selection in the first example; therefore it must be natural
selection in the second example as well.

Although quite compelling I think the above should be resisted in the
following way. Fitness attaches to the whole life cycle, not some
subpart of it. Why? Again the short answer relies on a commitment to
the fundamentality of reproduction. Reproduction is a reproduction of
the entire life cycle. It is true that fitness is often measured, as
in Kettlewell's case or in our hypothetical examples, by looking
at only a part of the life cycle. But from an evolutionary point of
view we are interested in this only when relative performance in this
part of the life cycle actually influences relative reproductive
success. Thus the first, but not the second, is a case of natural
selection. (Consider how Kettlewell's studies would have been
received by the evolutionary community if they had mirrored our second
hypothetical example rather than the first.)

In the preceding section we had to draw some fairly subtle
distinctions, but our conclusion is one with which the vast majority
of evolutionary biologists would agree. There is no such answer to the
question of this section. Many biologists define natural selection as
differential reproduction of heritable variation (see, e.g., Endler
1986). Many other biologists follow the tradition of quantitative
genetics and draw a sharp distinction between the ecological process
of selection and the evolutionary response to selection (see e.g.,
Falconer 1981). There are a large number of advantages to the second
approach, and I will follow it here. Thus we will arrive at a negative
answer to the question of this section.

First we must get clear on the relevant sense of heritability.
Recall § 2 above where we stated “Darwin's Three
Conditions”. They are: variation; heredity; and
differential reproduction. The notion of heritability relevant
here is the purely phenotypic, purely statistical notion developed by
Francis Galton (1869). That notion identifies heritability with
the regression of the offspring phenotype on the parental (or
biparental mean in the case of sexual reproduction), where both
phenotypes are presented as z-scores (i.e., set to mean = 0 and
standard deviation = 1). Intuitively the heritability is a
measure of how closely offspring deviation from the (offspring) mean
phenotypic value matches that of the parental deviation (from the
parental mean). That is, it measures the degree to which, for
example, taller than average parents produce taller than average
offspring. A value of 1 represents a perfect correlation between
offspring and parental deviations from their respective means, while a
value of 0 means there is no correlation, so that, for example, the
offspring of tall parents would not differ statistically from those of
short.

Unfortunately many people think that some sort of genetic definition
has supplanted this basic concept of heritability. In particular,
many would say that the Galtonian notion corresponds to the
“narrow sense” of heritability (h2),
h2 = VA/VT , where VA is
the additive genetic variance and VT is the total
variance. (VT is usually decomposed into
VA, VD—the variance due to allelic
dominance, and Ve—the environmental variance.
The latter is in fact a statistical catch-all, so it includes not just
variation due to environmental differences, but everything else.)
Even though this equation is very important and
we will revert to it shortly, we cannot accept this as a
definition of heritability for at least two reasons:
(1) Even for diploid sexually reproducing organisms that equation holds
only under certain genetic conditions (Roughgarten 1979); and (2) It
certainly is not applicable to pre-genetic or non-genetic
systems. But that would mean that the theory of evolution by
natural selection would not be applicable to the early stages of life
on this planet, nor to epigenetic inheritance, nor to cultural
transmission, nor to life elsewhere in the universe. Surely such
consequences are unacceptable and entirely unnecessary. Thus the
Galtonian notion of heritability is fundamental.

The motivation for saying that natural selection requires heritable
variation is clear. Only selection acting on heritable variation
will have evolutionary consequences. And since we are interested
in the concept of natural selection from a purely evolutionary point of
view (recall the introduction to this piece), we don't count
selection acting on non-heritable variation as natural
selection. (This seems analogous to the
argument in the last section saying that selection acting in a part of
the life cycle that is exactly counterbalanced later in the life cycle
should not count as natural selection.)

One response to this line of reasoning is to insist on the
importance of drawing a sharp distinction between the ecological
process of selection and the evolutionary process of response to
selection. The ecological process of selection, the domain of
ecological genetics, is complicated and difficult to study. The
evolutionary response to selection is the domain of population
genetics. It too is complicated and difficult. From a
purely strategic point of view it would seem wise not to conflate these
two complex processes into one.

I think most would agree with this bit of wisdom, but some would
counter by saying that it does not require a definition of natural
selection that is neutral on the heritability of the variation in
question. We can define ‘natural selection’ one way
or another and still agree on all of the facts. The argument for
one definition over the other will have to be made in terms of
simplicity, elegance, or some other non-empirical virtue of theoretical
constructs.

Let us illustrate the last point with a simple example, an example
that has been commonly used in the philosophical literature on units of
selection. The example is of heterozygote superiority, though any
example where the allelic effects on phenotype are non-additive would
do. (As would any number of cases involving non-additive
interactions among multiple genes.) There are two alleles at a
locus, A and a, and thus three
genotypes, AA, Aa, and
aa. For simplicity suppose that the two
homozygotes are lethal, i.e., they die before reproducing. Thus
all the matings are AaxAa.
Mendelism results in offspring of genotypes AA,
Aa and aa, in the ratio of
1:2:1. In a single generation the allele frequencies equilibrate
at 50:50 and stay there unless the fates of homozygotes
changes.

Although we criticized the genetic “definition” of
heritability as being derived and not general; it is useful for simple
genetic models like the one just described. In this example, once
the stable equilibrium is reached, the heritability, h2, is
zero. This is true because the additive genetic variation is
zero. (To apply the Galtonian notion of heritability to
this example, we would need to complicate it by specifying a
genotype-phenotype mapping, since that notion relates phenotypes.
We could do this, and provided Ve is not zero the Galtonian
value would be zero. But the point presently under
discussion would not be made stronger by this extra
complication.) So here we have a case where there is phenotypic
variation caused by genotypic variation, but the heritability of this
variation is zero because of the non-linear relationship between
genotype and fitness. How do we categorize the differential
reproduction that occurs in this example? Those who think that
natural selection requires the differential reproduction of heritable
variation would say there is no natural selection here. Those
following the quantitative genetics tradition would say that natural
selection is occurring, but that since h2 is zero the
response to selection is zero. (In accordance with the
fundamental formula of quantitative genetics, R =
h2S, where R is the response to
selection and S is the selection differential.)
But, it seems, there is no empirical difference between these two
points of view, so we need to decide between them on the basis of some
non-empirical reasons.

The seeming empirical equivalence between the two accounts offered
of our example is, in fact, illusory. Godfrey-Smith and Lewontin
(1993) have pointed out that there is an empirical difference between
an account of this case that says there is selection vs. one that says
there is no selection. (They make this point in the context of
discussing genic selectionism, which is committed to saying that there
is no selection in this case since the allelic fitnesses are the
same. For further discussion of this see Brandon and Nijhout
2006.) The empirical difference is that the first, but not the
second, can account for the within generation change in genotype
frequencies. At the start of each generation the three genotypes
are represented in the 1:2:1 ratio discussed above. Later in the
generation the homozygotes, both AA and
aa, die, so that 100% of the population is composed of
Aas. However, this difference is not an
evolutionary difference, since evolution is trans-generational
change. Our focus is on evolution. And it turns out
that the two models are not empirically equivalent with respect to
evolutionary predictions. The standard account, which says that
selection occurs each generation against the homozygotes, predicts a
stable equilibrium—one actively maintained by strong
selection. But the account that says that there is no selection
in this case has no basis to predict the same sort of stable
equilibrium. This is not apparent if one only considers
selection, because the genic selectionist recognizes the existence of
selection once one perturbs the population from its equilibrium and so,
it would seem, both models predict the same stable equilibrium.
However, once one brings in considerations of the interaction of drift
and selection (see next section) it has been shown that the models do
not give empirically equivalent predictions (Brandon and Nijhout
2006). This is because small perturbations from equilibrium will
have very different likelihoods of drift, because they will experience
quantitatively quite different regions within which drift vs. selection
is likely to dominate.

This example has a number of consequences (again see Brandon and
Nijhout 2006 and Brandon 2006). But for us the consequence is
this. To say that selection requires heritable variation is
factually wrong. When applied to a broad class of cases it makes
the wrong evolutionary predictions. And so we must reject that
view, and conclude that natural selection does not require heritable
variation.

Why should an entry on natural selection contain a section on drift?
One good reason is that natural selection and drift are co-products of
the same process, namely a probabilistic sampling process (Brandon and
Carson 1996, Matthen and Ariew 2002, Walsh et al. 2002). Thus,
although it is of crucial importance to separate selection and drift,
one cannot do so on the basis of process alone (contra Millstein
2002), one must do so on the basis on outcomes (Brandon 2005). Why is
this? If we think of fitness as a probabilistic propensity, then, as
we have seen, differential fitness is a necessary condition for
natural selection. Thought of this way, natural selection is a
probabilistic sampling process. We can characterize a continuum of all
possible fitness differences starting with maximal fitness differences
at one end of the continuum (i.e. where all fitness equal either 1 or
0, with at least some of each value), and minimum fitness differences
on the other (i.e., an equiprobable distribution). The two endpoints
are exceptional with respect to the relation of selection and
drift. At the maximal fitness difference end, one unlikely to occur in
nature, drift is impossible and selection is necessary. (See Figure
1.) At the finite set of minimal fitness differences at the other end
of the continuum, corresponding to absolute neutrality of the traits
under consideration, selection is impossible, because there are no
fitness differences. And drift is maximally likely, but not
necessary. Why not? Because the sample may be in accord with the
probabilistic expectations and thus no drift occur. (Imagine a
population with two alleles, A and
a, absolutely selectively neutral with respect to
each other, and at a 50:50 ratio. The next generation may also contain
the two alleles at the same ratio, if so, no drift has occurred.

Figure 1. The heavy horizontal line, with dotted center
section, represents the infinite number of possible fitness
distributions from Maximal Probability Differences (MPD—all
fitness = 0 or = 1, with some of both) on the left to the Equiprobable
Distribution (EP—all fitness the same) on the right. The
arrows emanating from the different descriptions of the modalities of
selection and drift indicate the areas of the distribution falling
under these descriptions.

But these two endpoints of this continuum are exceptional. More common
is surely the vast middle area where drift and selection are both
possible. In this middle ground we cannot say until after the fact
whether or not drift occurs, nor quantify the degree to which it
occurs. Prior to the fact we can only quantify the relative
likelihoods of selection and drift—they vary according to the
crucial quantity 4Ns. (Where N is the effective population
size and s is the selection coefficient, i.e. the strength of
selection. For discussion of 4Ns see any standard textbook on
population genetics, e.g., Roughgarden 1979, see also Brandon and
Nijhout, 2006.) The larger that quantity is, the larger N and the
larger s, the greater is the likelihood that selection will
dominate drift. And vice versa for small N and small s. Only
after the fact can one tell whether or not the probabilistic sampling
has gone in accord with the probabilistic expectations, or not. To the
extent that it has not, drift has occurred. Drift simply is the
deviation from probabilistic expectation. And since selection
itself is a probabilistic process there can be no purely
process-derived distinction between selection and
drift—attractive as that idea may be.

A more fundamental reason for a discussion of drift here in an entry
on natural selection is the view that drift is the zero-force
background against which evolutionary forces, including natural
selection, act (Brandon 2006). Just as in Newtonian mechanics one
could not properly understand the notion of gravitational force,
without understanding Newton's 1st Law, similarly one
cannot understand natural selection in evolutionary biology without
understanding the background against which it operates. Put in
other terms, drift provides the appropriate null hypothesis against
which to test any selection hypothesis. Unfortunately this is not
always well understood. Indeed this way of thinking about
evolution stands some canonical versions of evolutionary theory on
their heads. For instance, those who would take the
Hardy-Weinberg Law as a Zero-Force Law of evolution (see, e.g., Ruse
1973, and Sober 1984, but also many standard textbooks in evolution)
view stasis as the default state of evolutionary systems, with some
evolutionary force needed to move (i.e. evolve) them. Without a
net force, no net change. But all modern methodology in molecular
evolution is predicated of the truth of just the opposite idea, namely
that left alone evolutionary systems drift. Drift is the default
state. So that, for instance, neutral alleles in different
populations differentiate from each other. But this molecular
truth is iterated throughout the biological hierarchy. Once
speciation occurs, species differentiate (drift apart) as a null
expectation. Which is not to say that natural selection cannot
produce evolutionary change. Of course it can. But if we
are to properly recognize it, we must be able to recognize the
signature of selection and differentiate it from drift's
signature (see, e.g., Bamshad and Wooding 2003). Change in
evolution is a heterogeneous category.

Stasis, on the other hand, is largely homogeneous. Long-term stasis
can only occur by natural selection.